Culturing Science – biology as relevant to us earthly beings

Posts Tagged ‘Microbes

DMS(P): the amazing story of a pervasive indicator molecule in the marine food web

This post was chosen as an Editor's Selection for ResearchBlogging.org

Dimethylsulfide.  Does that word mean anything to you?  “Why yes,” you organic chemistry nerds may say, “It clearly is a molecule of sulfur with two methyl groups attached.”  That’s as far as I could have gotten – until this past week, when I inundated myself with information on dimethylsulfide (DMS) due to a paper published in Science.  Now I’m enlightened – what a wonderful molecule!  Let me spoil it for you: it is simultaneously a defense mechanism, a chemical cue pervasive throughout the marine food web, and an effector on the earth’s climate.  (See illustration at bottom of post for summary.)  That’s right.  Just a sulfur molecule with two methyl groups attached.  Now let’s back up a bit.

DMS is a sulfur compound that accounts for 50-60% of the total natural reduced sulfur flux to the atmosphere (even more than either volcanoes or vegetation).  While sulfur in the atmosphere can cause acid rain, it is also very important, as it helps form clouds.  In order for water to transition from a gas to liquid in the atmosphere, it needs a small particle in the air to adhere onto, known as a cloud condensation nucleus.  Sulfur oxide, which can be derived from DMS, is one of these particles.  Clouds not only carry our precipitation, but help to reflect sunlight (and thus heat) back into space, affecting our planet’s climate.

After the realization of its importance as a cloud condensation nucleus, scientists began to look for DMS’s planetary source and found that 95% of the atmospheric DMS originates in the oceans – but from where?  As illustrated in my figure, it is actually formed in certain species of phytoplankton and released when cells leak, most often due to herbivory by other organisms.  The phytoplankton itself actually makes a molecule called DMSP (dimethylsuphoniopropionate, if you must know).  When its cell wall begins to break down, stores of DMSP (from an unknown location within the cell) and an enzyme, DMSP-lyase, are released into the surrounding water.  This DMSP-lyase removes the P-group, leaving us with our favorite molecule of the day, DMS.

In 1987, the CLAW hypothesis (named for its authors) was put forward by James Lovelock and a handful of his lackeys to support his infamous Gaia hypothesis which suggests that microorganisms regulate the Earth’s climate to maintain conditions suitable for life.  CLAW hypothesized that levels of DMSP and its P-cleaving enzyme in phytoplankton are regulated by light and temperature, with greater amounts of DMSP produced when it gets warm in order to send more DMS into the atmosphere, deflecting sunlight and reducing global temperatures.  However, like most support for the Gaia hypothesis, this idea requires that phytoplankton act altruistically, releasing the DMS for the good of the planet, which does not make much sense in light of natural selection.  (A good review of this and the above sections can be found in this paper by Rafel Simo.)

A 2001 MEPS paper by Kathryn Van Alstyne and others provides evidence that the release of DMSP and DMSP-lyase by phytoplankton is actually a chemical defense mechanism.  After DMSP-lyase activity, the resulting products are DMS and acrylase or acrylic acid.  The authors found that acrylic acid deterred grazing by two species of sea urchins on algae, and they suggest that this is due to an aversion to acidity by the urchin itself or that the acid irritates its gut microbes.  While the evidence is not directly causative, as the authors showed a reaction to acrylic acid and not to DMSP-produced acrylic acid in vivo, it does suggest (with other evidence) that the important part of this reaction to the phytoplankton is not DMS, but rather its byproduct.

Fig. 1 from Van Alstyne et al. (2001), showing the DMSP-lyase reaction

Smaller grazers, such as isopods, had no reaction to the acrylic acid in that paper.  But a paper published in Science this week (July 16 2010) by Justin Seymour, Rafel Simo, and others looks into the effects of DMSP on the smallest grazers: microbes.  Using “microfluid technology” (see details at end of post), the researchers measured the strength of attraction of 4 different types of microbes (7 species) to varying concentrations of DMSP, DMS, DMSO (dimethylsulfoxide, a DMS and DMSP degradation product), GBT (glycine betaine, a molecule analogous to DMSP in structure and function), and artificial seawater (as a control).

  1. Each of the 3 species of autotrophic plankton reacted differently to DMSP in the water.  The algae Micromonas pusilla showed strong attraction to DMSP, taking it up presumably as a carbon and sulfur source.  The cyanobacterium Synechococcus sp. showed no reaction.  Most strangely, the algae Dunaliella tertiolecta moved very strongly toward DMSP, but not to assimilate it directly; rather, it cleaved the molecule into DMS extracellularly and potentially assimilated that molecule instead.  The authors do not know why this action occurs.
  2. Two species of bacteria, Pseudoalteromonas haloplanktis and Silicibacter sp., each moved toward the DMSP for assimilation as part of their carbon and sulfur requirements.
  3. Two consumers, one a herbivore to eat the algae itself (Oxyrrhis marina) and the other a bacteriovore which strove to eat the bacteria consuming the DMSP, each showed positive chemotaxis and moved toward the DMSP source.

This last part is the most interesting: these two microbe species use the DMSP as a chemical signal that there is food around.  Out of all the molecules that could leak from the burst cell and indicate prey, it is this very molecule, DMSP, that does the trick.

But wait: didn’t the 2001 paper I just wrote about suggest that DMSP is a chemical defense of phytoplankton?  What is it doing drawing in its own predators?  The authors suggest that previous studies have flawed experimental design, releasing far too much bulk DMSP into the environment in contrast to their own “microfluid technology.”  Previous studies, such as a 1997 Nature paper by Gordon Wolfe and a 2003 paper by Suzanne Strom, found that O. marina has a higher tolerance to digesting DMSP and is less repelled than other species.  More work should be done in order to get to the root of this contradiction.

Thus far, we have DMSP attracting bacteria to consume the DMSP itself, drawing in an herbivore to consume the DMSP-producer, and a bacteriovore attracted to the DMSP in order to find its own bacterial prey.  This is not the end of the story, as DMSP is a prey indicator at higher trophic levels as well.  A 2008 Science paper out of UC-Davis and UNC found that planktivorous fish use DMSP as a foraging cue, aggregating near DMSP hotspots.  Furthermore, Gabrielle Nevitt reviewed literature in 2008 on seabirds (Order: Procellariiformes) using DMS as an olfactory cue to identify patches of its own prey, fish and squid, feeding on the zooplankton and its phytoplankton prey.  A similar pattern has also been found in seals and whale sharks.

The evolutionary implications of this are astounding.  It seems as though many molecules released from a leaky phytoplankton cell could be used as indicators of these clusters of consumption.  However, DMSP has something special: sulfur.  We all know that smell, and perhaps it is this stinkiness that has allowed it to become such a pervasive indicator throughout the marine food web.  In her review, Nevitt discusses the evolution of DMS-sensitivity in seabirds, and using phylogenetic trees, shows that only the species that are reared in dark burrows, relying on smell alone to identify food, currently have DMS-sensitivity.  How did this apparent convergent evolution occur?  Is it convergent?  (I have no answers to these questions.)

Are there any implications for climate in these findings, as DMSP is indirectly responsible for increased albedo (sunlight reflection) in our atmosphere?  I doubt that there are any direct consequences that we can enumerate.  As all biogeochemists know, the stuff of the air frequently comes from the stuff we live on and in: soil and water.  This is simply another tie to the way microbes and abiotic stuffs relate to climate-regulating molecules.  The authors of this week’s Science paper note that “microbial behaviors, played out over microscale chemical landscapes, shape planktonic food webs while potentially influencing climate at global scales.”  DMS as a prey cue should create a positive feedback loop, drawing more herbivores to open more cells and leak increasing DMSP, which in turn draws more herbivores.  Some studies show varying ties of DMSP production to species, light, temperature and salinity (review by Stefels et al. here), but it seems to me that the DMS-as-prey-cue and DMS-as-climate-regulator processes are unlinked, so would not work together in any predictable way.

If you take nothing away, take this: sometimes the universe is more connected than we can imagine.

(Sidenote: should I give up strict science and become a science illustrator?)

NOTES ON MICROFLUID TECHNOLOGY:
The idea behind this technique is that microbes inhabit a “dynamic and patchy nutrient landscape” in which nutrient levels vary over micrometer scales.  The microfluidic device is a chamber designed with the “objective of creating a diffusing band of chemoattractant, to simulate an ephemeral, microscale nutrient patch.”  There is a chamber in the center into which fluorescence-labeled chemoattractant is added to the desired concentration, and then input is cut off.  Thus the chemical will dissipate slowly through the closed chamber, trying to imitate the open ocean.  The researchers then add their microorganisms, and measure their distribution and the distribution of the fluorescent chemical.  This allows the researchers to track the intensity and location of the chemical, as well as the behavior of single organisms.

This information is from a paper in Limnology and Oceanography: Methods by J.R. Seymour, T. Ahmed, and R. Stocker entitled “A microfluidic chemotaxis assay to study microbial behavior in diffusing nutrient patches” (2008: 6 (477-488)).  A pdf copy of this paper is available on Roman Stocker’s webpage, here (pdf warning!).

Here’s a picture of the device, thanks to Roman Stocker.  The blue tube is the microbe input, the green tube is chemical input, and the red tube is for drawing out waste.  It sits on top of a microscope.

DeBose, J., Lema, S., & Nevitt, G. (2008). Dimethylsulfoniopropionate as a Foraging Cue for Reef Fishes Science, 319 (5868), 1356-1356 DOI: 10.1126/science.1151109

Nevitt, G. (2008). Sensory ecology on the high seas: the odor world of the procellariiform seabirds Journal of Experimental Biology, 211 (11), 1706-1713 DOI: 10.1242/jeb.015412

Seymour, J., Simo, R., Ahmed, T., & Stocker, R. (2010). Chemoattraction to Dimethylsulfoniopropionate Throughout the Marine Microbial Food Web Science, 329 (5989), 342-345 DOI: 10.1126/science.1188418

Simó, R. (2001). Production of atmospheric sulfur by oceanic plankton: biogeochemical, ecological and evolutionary links Trends in Ecology & Evolution, 16 (6), 287-294 DOI: 10.1016/S0169-5347(01)02152-8

Stefels, J., Steinke, M., Turner, S., Malin, G., & Belviso, S. (2007). Environmental constraints on the production and removal of the climatically active gas dimethylsulphide (DMS) and implications for ecosystem modelling Biogeochemistry, 83 (1-3), 245-275 DOI: 10.1007/s10533-007-9091-5

Van Alstyne, K., Wolfe, G., Freidenburg, T., Neill, A., & Hicken, C. (2001). Activated defense systems in marine macroalgae: evidence for an ecological role for DMSP cleavage Marine Ecology Progress Series, 213, 53-65 DOI: 10.3354/meps213053

G. V. Wolfe, M. Steinke, & G. O. Kirst (1997). Grazing-activated chemical defence in a unicellular marine alga Nature, 387, 894-897

Written by Hanner

July 19, 2010 at 8:19 am

Microbe biogeography: the distribution, dispersal and evolution of the littlest organisms

EDIT: This post was selected as a runner up for the PLoS ONE Blog Pick of the Month. Thanks, PLoS! Check out the winner: Greg Laden’s great post on how the victims of Vesuvius died.

ResearchBlogging.orgIn any high school biology class1, we learn that isolation is key to the evolution of species.  For example, take Australia, where an array of marsupials such as koalas and kangaroos reproduce like no other animals on the planet.  Isolation on a continental island allowed ancestral marsupials to evolve gestation via pouch, a trait which was retained as these animals later evolved into multiple (cuddly) species.  In other words: an event that happened in the past resulted in the organisms we see today, or the history of a species influences its current form and life history.

We attribute the distribution of species on this planet, also known as biogeography, to these sorts of historical events.  Organisms evolved, and continue to evolve, the way they do due to historical circumstances out of their control, creating the biodiversity of our world.  The idea of biogeography is generally attributed to Lamarck, and throughout the late-18th and early-19th centuries (pre-Darwin, mind you), scientists suggested many reasons for the non-uniform distribution of organisms, with Lyell summing up these historical factors as a combination of environment and dispersal through migration, passive (e.g. seeds carried in the wind) or active (e.g. elephants walking across the plain).

It's hard to find images for these kinds of posts, ok? Cut me some slack. By the way, image (c) Hannah Waters 2010

However, not all organisms seemed to fit this pattern.  Scientists at this time observed that, while polar bears were limited to the arctic and monkeys to warm climes, organisms such as fungi, sponges, algae and lichens were far more ubiquitous.  The botanist Kurt Sprengel, in summary of a common thought, wrote that organisms of “lower organization” must have greater ability to disperse, allowing them to colonize more broadly and thrive where “circumstances propitious to their production occur.”  (For a full history, see Maureen O’Malley’s commentary in Nature Reviews Microbiology.)

In 1934, the Dutch biologist Lourens Baas-Becking revived this idea, with the thought that the typical explanations of biogeography do not fit with the world of microorganisms.  He saw the same species of microbe living in different places on the globe and in variable environments.  Thus, he posited that historical factors such as isolation and environment could not be the forces determining microbial distribution,  but rather that “everything is everywhere; the environment selects.”  The small size and abundance of many microbe species allowed them to be easily dispersed in water, on wind, on the bodies of animals, spreading them all over the planet.  Many microbes can also lie dormant for a long time until conditions improve, or until the “environment selects” them.  This would, in effect, create what’s been termed a “seed bank” of microbes, where all microbes are in all environments at the same time, lying in wait for environmental conditions to favor their proliferation.

A generic microbial community. Source: Frank Dazzo, Center for Microbial Ecology, Michigan State University

For most of the 20th century, this so-called “Bass-Becking Hypothesis” was widely accepted, but in the past few decades has been hotly debated.  In 2004, Tom Fenchel and Bland Finlay compiled a literature review in Bioscience in favor of the hypothesis, arguing that “habitat properties alone are needed to explain the presence of a given microbe, and historical factors are irrelevant.”  They reviewed studies which showed the ubiquity of microbe species with fewer habitat requirements (generalists, if you will), as well as microbe species that are environmentally specific but are found in their preferred habitats on many continents.  Of note is a 1997  Oikos study that they themselves published, wherein they found 20 living microbe species in a lake sample.  Upon altering conditions (such as food source, temperature, acidity, and oxygen levels), they were able to revive an additional 110 species – evidence supporting the idea of a “seed bank” of microbes.  The authors do note that this theory may only apply to the most common microbe species, since not all are able to dessicate and revive – but perhaps this ability is what made them so widespread in the first place.

One caveat with this study is that the authors advocate for a phenotypic analysis of microbes.  While the ability to study DNA was a huge benefit to the field of microbiology, the authors do not agree that this is useful due to the wide genetic variability even within a single microbial population, and thus rely on morphology to describe species instead of genetic analysis.  A 2006 review, including genetic analyses, found that things aren’t so cut and dry.  The authors cite a number of studies showing reproducible genetic differences within microbe species even along a 10-meter transect in a marsh.  In two hot springs thousands of kilometers apart, despite living in the same environment, two species of bacteria (Synechococcus and Sulfolobus) showed significant genetic differences.  This shows that isolation alone can affect genes, and thus ultimately species, “overwhelming any effect of environmental factors.”

Both reviews note that there is not enough data out there to draw strong conclusions; the 2006 study was relying on 10 articles alone to determine distance and environmental signficance.  To me the differences in these studies come down to how one defines a “species.”  Typically, we differentiate species based on an organism’s ability to produce fertile offspring with another – if they can, they are the same species.  (There are many caveats to the “species problem” beyond my scope right now.  For a really thorough write-up, see this post from the Wild Muse.)  However, most microbes reproduce via cell division, and genes can be transferred horizontally despite “species” boundaries.  So how do we even define a microbial species in the first place?  If we’re looking at evolution alone, it would seem that genetic differences even within microbes that are commonly described as the same species morphologically would be meaningful, as these genetic differences put them on the path to become novel species.

One major question that the idea of “everything is everywhere” brings up is: how do microbes evolve in the first place?  If these organisms are relatively free from the external pressures of isolation and environment, going locally extinct or reviving based on their surrounding conditions, evolution must take an incredibly long time.

I could not find a paper on biogeography and microbial evolution; however, a paper in PLoS published in April 2010 looked at the biogeography and large-scale evolution of phytoplankton in the ocean.   In light of questions I’m asking here, oceanic plankton and microbe communities are very similar.  They are both small organisms  primarily dispersed passively, by ocean currents in the case of plankton.  The ocean hosts a wide variety of environments, and plankton are also generally considered to be everywhere at once.  While it is not ideal, I will use this planktonic model to look at biogeography and evolution in a more specific system.  (Well, as specific as you can get with the ocean…)

A generic planktonic community.

Just as the determinants of microbial biogeography haven’t been concluded, the same is true of plankton.  In this study, the authors sampled planktonic communities in two very different ocean environments: subtropical/tropical oceans, characterized by similar conditions throughout a wide geographical range, highly stratified ocean layers, and nutrient-poor surface waters, and sub-Arctic waters, characterized by high vertical mixing and high nutrient levels across the water column.  They compared 250-ml samples pairwise from each of the oceanic habitats and found that the planktonic communities were “strikingly dissimilar.”  However, when they increased their sample size 100-fold to 25 liters, they found that these contrasting ocean environments shared 76% of their total species pool!  This effect is surely found in many microbial studies: when comparing diversity between smaller plots, you are more likely to find a difference.  But an increase in plot size, even within the same environment, will find more similarities.  (Which is a more meaningful measurement is another question… I’d be happy to hear your comments on that one.)

To look at the evolution of phytoplankton, the authors took core samples from four distinct geographic environments and then identified fossil diatom species within from 240 million years ago to the present, generating “community assemblages” of diatoms through time.  They then compared these communities assemblages with environmental factors: global CO2 concentrations and oceanic upwelling strength.  The authors found that, despite “local determinants such as regional current systems, terrestrial nutrient inputs, atmospheric deposition, physical mixing, etc.,” global climate measures largely predicted the diatom community assemblage, with many species recovering after local extinction.  That’s right: even after the extinction of a species, when preferable environmental conditions returned, so did the diatom.

This study provides a clue regarding the importance of environmental conditions to the global distribution of abundant, passively dispersed organisms.  What is also interesting is that the same diatom species were found again and again over the course of 240 million years.  Their ability for high dispersal and recovery of species enables planktonic communities to evolve “slowly and gradually” over time.

But clearly they have evolved: plankton (and microbes) are incredibly diverse clades.  The question to look at now is how is evolution driven in highly dispersed organisms?

And thus, as usual, they are the tiniest organisms that force us to broaden our view on basic tenets of biology.  Just as horizontal gene transfer did for traditional natural selection, now microbial dispersal does for the evolution of species.

It does give me a great deal of hope regarding life on this planet: the possibility that there is a cache of microbes waiting around for the perfect conditions, even ones not suitable for us.  As my father, Dennis P. Waters (who needs a blog), once put it, “As long as there’s bacteria, there’s hope.”

1That is, in one where evolution is taught at all…

Cermeño, P., de Vargas, C., Abrantes, F., & Falkowski, P. (2010). Phytoplankton Biogeography and Community Stability in the Ocean PLoS ONE, 5 (4) DOI: 10.1371/journal.pone.0010037

Fenchel, T., & Finlay, B. (2004). The Ubiquity of Small Species: Patterns of Local and Global Diversity BioScience, 54 (8) DOI: 10.1641/0006-3568(2004)054[0777:TUOSSP]2.0.CO;2

Martiny, J., Bohannan, B., Brown, J., Colwell, R., Fuhrman, J., Green, J., Horner-Devine, M., Kane, M., Krumins, J., Kuske, C., Morin, P., Naeem, S., Øvreås, L., Reysenbach, A., Smith, V., & Staley, J. (2006). Microbial biogeography: putting microorganisms on the map Nature Reviews Microbiology, 4 (2), 102-112 DOI: 10.1038/nrmicro1341

O’Malley, M. (2007). The nineteenth century roots of ‘everything is everywhere’ Nature Reviews Microbiology, 5 (8), 647-651 DOI: 10.1038/nrmicro1711

Written by Hanner

June 18, 2010 at 10:41 am

Animals without oxygen and their implications for the evolution of life

ResearchBlogging.orgIt’s been a slow few weeks around here at Culturing Science.  It’s due to a little bit of writer’s block, but mainly it’s just the beautiful weather keeping me outdoors and away from the computer.  Hopefully you’ve been outside so much that you haven’t noticed.

But today my dream article was published: microorganisms, extreme environments, evolution, and daydreaming all rolled into one.  I couldn’t resist but write it up in an excitement-driven fury.  (The 90 degree weather in Philadelphia is also a little too hot for my taste.)

Are you sitting down?  Today scientists from the Polytechnic University of Marche (Ancona, Italy) and the Natural History Museum of Denmark published their discovery of the first multi-cellular animals found to survive without oxygen.  You’ve probably heard of Archaea or Bacteria species which are able to survive in extreme temperatures, acid, or sulfur-rich environments – places we wouldn’t dream of living.  And the world at large is fascinated by them for this reason.

For this study, the scientists collected sediment core samples from the L’Atalante basin in the Mediterranean.  This basin is completely anoxic (oxygen-free), with a salty layer of brine above forming a physical barrier preventing any oxygen from reaching the area.  In the sediment, they found traces of animals from three phyla:  Nematoda, Arthropoda and Loricifera.

However, as all the animals were dead upon analysis, they had to confirm that these animals were in fact living in the sediment, and hadn’t simply settled there in a “rain of cadavers”  (What poetry!) from oxygenated areas of the sea.  They treated the specimens with a stain that binds to proteins – presumably dead animals would have fewer proteins due to decomposition.  In the figure to the right, we see little protein in the Arthropoda (a) and Nematoda (b) images.  However, the Loricifera (c) specimen is bright pink, indicating protein.  The arthropod and nematode species are thus probably dead bodies or shed exoskeletons – but the Loriciferan (unstained in f) shows promise of actual life in the oxygen-free sediment.

After staining more specimens, the researchers also noticed eggs (d and e) within the bodies of the Loriciferans.  This is a novel find because it suggests that these animals do not just spend part of their lifecycle in the anoxic sediment, but live without oxygen for their entire lives, including reproduction.  They additionally found exoskeletons from young Loriciferans (g) suggesting that these eggs grow up in the sediment as well.  While it would still be a new discovery to science if we found animals that live part of their lives in anoxic conditions, the fact that they spend their entire lifecycles down there raises many more questions and expands our definition of life on this planet.

To further confirm that these bugs are living in the sediment, the team gathered fresh sediment samples and added radioactive protein to see if the Loriciferans would eat it.  They traced this radioactivity and found that the animals had incorporated the radioactive substrate into their bodies providing final evidence that these guys are in fact living without oxygen.

So what’s the big deal about a multicellular organism living without oxygen?  Why am I nearly peeing myself over this?  We already know about single-celled organisms can live in extreme conditions.  Why is this so exciting?

It makes sense that single-celled organisms would be more likely to survive in weird places because they can adapt to environments more easily.  They only have one cell to take care of, so if that one cell is viable, they’re fine.  In addition, single-celled organisms are more likely to transfer genes between one another, allowing adaptations to spread more quickly.  But it was assumed that we don’t find multicellular life in extreme conditions because more complex life simply could not exist there.

But now we have found a multicellular animal that can survive without oxygen.  And the million dollar question: how did it evolve that way?  In their findings, Danovaro et al. mention that the Loriciferans don’t appear to have mitochondria, which are found in oxygen-consuming animals, but rather hydrogenosomes, which are found in some single-celled organisms living in extreme environments.  This presents the possibility of endosymbiosis – or the incorporation of one organism into the other.  Endosymbiotic theory is widely accepted to explain mitochondria and chloroplasts in cells; perhaps this occurred another time for the hydrogenosomes of the Loriciferans.  This suggests that maybe this is not as rare of an event as we thought – who knows what other organelles have evolved this way, including ones we haven’t identified yet.

This finding has implications for how we think about the evolution of life on earth.  We humans are obsessed with ourselves; since we breathe oxygen, it’s often assumed that life on earth evolved once oxygen was around.  The discovery of these non-oxygen-breathing animals provides evidence that multicellular life could have risen prior to oxygen, supporting evidence that early life evolved in highly acidic conditions.  (For more on this, see Marek Mantel and William Martin’s commentary on this paper.)

But let’s get down to the real business: let’s talk about space and aliens.  Thus far, we have been primarily searching for alien life based on oxygen because we have lacked proof that complex life can exist that isn’t oxygen based.  The only life we know – us – is oxygen based, providing no other models of life besides planets with oxygen.  The prior knowledge of only single-celled organisms living in non-oxygen based environments suggested that intelligent life cannot exist in those systems.  And while I wouldn’t consider Loriciferans (also known as “brush-heads”) intelligent, they do suggest that non-oxygen substrates can support higher life.  So when looking for aliens, let’s stop being so anthropocentric.  Life can survive without oxygen.

Danovaro, R., Dell’Anno, A., Pusceddu, A., Gambi, C., Heiner, I., & Kristensen, R. (2010). The first metazoa living in permanently anoxic conditions BMC Biology, 8 (1) DOI: 10.1186/1741-7007-8-30

Written by Hanner

April 7, 2010 at 2:41 pm

Photosynthetic Evolution: how 2 organisms gained or lost the ability to eat sunshine

9/13/2010 Update

New research has come out that changes the story told below. Wägele et al. sequenced cDNA transcripts from RNA produced by slugs dependent on their plastids alone, and did not find the RNA to produce the proteins for plastid use in any meaningful quantity. But the slugs aren’t just using the proteins they got upon original ingestion; we simply do not know what is happening.  For a thorough write-up, I highly recommend this post from The Spandrel Shop entitled “Solar Sea Slugs: part plant, part animal… or not?”

Original post (01/20/2010):

ResearchBlogging.org

The variety of protist life -- from Finlay, B.J. & Esteban, G.F. Protist, 149, 155-165 (via the British Society of Protist Biology).

Biologists and taxonomists love to put organisms into categories to help us organize the complicated living world.  I grew up on the 5 kingdom system of classification: plants, animals, fungi, bacteria and protists. The first four categories seemed simple enough, but the term “protists” always confused me.  This kingdom seemed to be a dumping ground for all the single-celled organisms that we didn’t know what to do with, ones that had evolved so far from their ancestors that their origins were unknown.

I’ve stumbled upon two fascinating articles about such animals that are out of place.  The first is about microorganisms that were once photosynthetic — and thus evolved with the cyanobacteria and plants — but no longer go through photosynthesis.  The second is about a sea slug that has developed the ability to photosynthesize, or harvest energy from the sun.  Imagine stumbling upon these animals for the first time.  The former would be placed in the animal kingdom due to its heterotrophy, or tendency to get its nutrients from food.  The latter would be baffling: is it some freak highly-organized plant, or an anomalous, energy-producing animal?  Thanks to our increasingly understanding of evolution, scientists have been able to figure out where these strange creatures came from.

The first story is about evolution driven by competition for food between many species of microorganisms.  In terms of energy acquisition, I usually think about two categories of organisms: the heterotrophs, which get their energy from eating, and the autotrophs, which create their own energy from outside inputs such as the sun.  But there are also the mixotrophs, which are able to do both.  To be a mixotroph!  How wonderful would it be to get energy from standing under the sun if you wanted, but you could also be able to eat a hearty meal for the same gain!  On first thought, this appears to be the best life strategy, allowing an organism to get energy whatever way is easiest at the time.

Scientists from the University of Potsdam in Germany and the Austrian Academy of Scientists propose that, in some circumstances, having both strategies may be too much (open access paper here).  In order to be a mixotroph, the organism needs to fit all the machinery required for both processes inside its single cell, increasing its size.  A bigger mixotrophic cell not only loses access to smaller food items, such as ultramicobacteria, but also has to compete with larger heterotrophic organisms, which are solely dedicated to eating and thus can do so more efficiently.  These scientists created a model showing how, under low-light conditions, it would be energenically beneficial for mixotrophs to be rid of their chloroplasts and other organelles needed for photosynthesis so that they could become physically smaller and have access to the smaller foods out of the range of other heterotrophs.  Thus, we have animal-like organisms that evolved from plants.

The second story is about a sea slug, Elysia chlorotica, which has gained the ability to photosynthesize.  It did not evolve this trait in the traditional sense, but rather picked it up from another organism.  The slug’s green color is not self-made, but is present due to its collection of chloroplasts, the photosynthetic center of a cell, from its prey.  Due to an unknown mechanism, the slug is able to hoard only the chloroplasts of its algal food source Vaucheria litoria.  Not only that, but it uses these chloroplasts to go through photosynthesis itself, which it can continue to do 5 months after it last ate V. litoria.  (And this is a slug that only lives for 10 months total.)

This is not as simple as it sounds, however.  You need more than chloroplasts to photosynthesize; you also need genes to encode all the specialized proteins needed to make sunlight into energy!  The big question regarding these slugs was: where did they get these genes?  Scientists working together from Maine, Korea, Iowa and Texas (paper here) compared sections of the nuclear DNA between the slug and its algal food and found identical segments, suggesting that the slug had not evolved these genes on their own, but had acquired them through horizontal gene transfer, or a transfer of DNA from an origin other than one’s own parent.  In this case, they suggest, a segment of the algae’s DNA broke off and joined the slug’s own DNA, an incredibly rare event.  This gene acquisition was so beneficial that it spread through the population, causing E. chlorotica all over the oceans to hoard the chloroplasts of their prey.  And there ya have it, folks: a photosynthetic animal.

Ain’t this a wonderful world we live in?

Learning about the histories of these organisms makes me drool, thinking about the uncategorized protists out there.  What kind of stories do they have to tell?

de Castro, F., Gaedke, U., & Boenigk, J. (2009). Reverse Evolution: Driving Forces Behind the Loss of Acquired Photosynthetic Traits PLoS ONE, 4 (12) DOI: 10.1371/journal.pone.0008465

Rumpho, M., Worful, J., Lee, J., Kannan, K., Tyler, M., Bhattacharya, D., Moustafa, A., & Manhart, J. (2008). Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica Proceedings of the National Academy of Sciences, 105 (46), 17867-17871 DOI: 10.1073/pnas.0804968105

Written by Hanner

January 20, 2010 at 10:43 pm

How dirt affects global atmospheric carbon dioxide (Wingate et al. 2009, PNAS)

This post was chosen as an Editor's Selection for ResearchBlogging.org I have a tendency to root for the underdog.  I rooted for the Phillies throughout the 90s, when my heroes Lenny Dykstra and Darren Dalton could rarely lead them to a win.  It’s a mixture of a desire for upheaval, that the unexpected can happen, as well as pure sympathy for the ones who always lose.

Do you know who always loses in science?  Dirt.  No one cares about it.  I mean, it’s a mixture of poop and rotting plants and animals.  It harbors fungus and worms and bacteria.  And while it is generally accepted that it has an important role to play, it tends to be overlooked because it’s just not all that exciting on the surface.  Why study ground up brown stuff when you can study WHALES or CANCER?

That’s why I love it when dirt wins, as it does in this early-access article from PNAS entitled “The impact of soil microorganisms on the global budget of δ18O in atmospheric CO2” (doi:10.1073/pnas.0905210106).  The closest I’ve heard soil come to being included in the climate debate is the possibility of pumping liquid carbon dioxide deep beneath the earth’s surface to sequester it: not the most dignified of positions.  But this article provides evidence that it is more involved than that, and helps to mollify some discrepancies between prior models and observed measurements in carbon dioxide.

One of the most common ways to trace the origins of oxygen in the atmosphere is through isotope analysis.  Carbon dioxide cannot dissolve in water on its own, but needs to be made into the ions HCO3+ and H+ so that it can be transported in fluids.  An enzyme, carbonic anhydrase (CA), switches carbon dioxide between its dissoluble and soluble forms, and is found in both plants and animals.  It is an incredibly important enzyme for both respiration and photosynthesis.  If CO2 were ionizing on its own, without an enzyme, it would take far longer, and the systems would be far less efficient.  However, it leaves a mark: a heavy isotope of oxygen.  The new CO2 molecule, built by CA, adds 2 more neutrons to oxygen, creating a δ18O isotope which we can trace, thus tracing the activity of CA.

Since δ18O is a heavy isotope compared to oxygen-16, the normal form, it preferentially remains in leaf tissues during transpiration and evaporation.  Eventually these leaves die and fall to the soil, where they are broken down.  The amount of δ18O in the soil has traditionally been used as a measurement of plant photosynthesis.  The possibility of CA activity in soil has been disregarded bcause of the high levels of δ18O in just the top few centimeters of soil, indicating that it is due just from decomposing leaves.

The 18 authors of this paper decided that this assumption wasn’t good enough.  What if microorganisms are creating δ18O in the soil due to their own CA activity?  What would this mean for the overall oxygen budget?  First of all, it would mean that plant photosynthesis would have a lesser role.  It could also change the estimations of photosynthesis vs. respiration in our atmosphere, since the microbes could be either photosynthetic algae or cyanobacteria, or respiratory little buggers.

The authors took the measurements of δ18O at different soil depths from 7 different major earth ecosystems from the field, and also created the artificial conditions in chambers with to determine if δ18O levels differed between the two.  They also used this “chamber-flux” data to estimate different rates of δ18O creation under different CA catalyzation levels.  These data showed that naturally measured δ18O levels were greater than the control levels without CA: up to 300x in the more productive ecosystems!  This provided clear evidence that δ18O is being created by soil microorganisms through CA enzymatic activity on their own.

This information was consistent with  previously observed and modelled δ18O curves, shown in the figure above.  The top half shows the observed δ18O levels in dark blue dots, with the modelled line in black, with the frames increasing in CA activity from left to right.  In the right frame, with CA activity at 300x the left frame, the modeled and observed δ18O creation rates overlap.  (The curve is based on latitude — northern latitudes, with much vegetation and high photosynthesis on the left, decreasing in photosynthetic production as we move southwards.)  This provides more evidence that CA is present in soils, as in an ideal world, observations and models will match up.

The bottom half of the figure is based on the concept of isoflux.  This is a measurement of CO2 in the atmosphere, with positive values indicating photosynthesis, while negative values indicate greater respiration, which removes CO2.  The “soil invasion” line, in orange, goes from showing no-change in the no-catalyzation scenario, to absorbing nearly as much CO2 as respiration.

So, really, what is this paper saying?  First of all, don’t ignore the dirt!  Soil microbes may be small, but they are vast in number and can really have an impact on our element cycling.  More than anything, this paper helps to adjust previous models.  It suggests that the soil may be more of a carbon dioxide sink that we previously thought, because we now have evidence that respiration is taking place due to this increase in δ18O from CA use.

To me, what this paper really shows is how little we know.  We’re trying to model oxygen and carbon in the atmosphere and earth, and there’s so little way of knowing.  If it weren’t for this enzyme, carbonic anhydrase, that happens to incorporate a heavy oxygen isotope, where would we be?  Modelling is important, don’t get me wrong.  But it is also incredibly frustrating because we really don’t know enough to create very accurate models.  This paper is a little slice, sure; but we could be missing huge impacts just because they are untraceable.

Wingate, L., Ogee, J., Cuntz, M., Genty, B., Reiter, I., Seibt, U., Yakir, D., Maseyk, K., Pendall, E., Barbour, M., Mortazavi, B., Burlett, R., Peylin, P., Miller, J., Mencuccini, M., Shim, J., Hunt, J., & Grace, J. (2009). The impact of soil microorganisms on the global budget of 18O in atmospheric CO2 Proceedings of the National Academy of Sciences DOI: 10.1073/pnas.0905210106

Written by Hanner

December 24, 2009 at 11:31 am

Posted in Journal Article

Tagged with , , ,

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